Distribuição espacial de enteroparasitas em crianças escolares na cidade de Guarapuava, Estado do Paraná, Brasil
Maria Luisa Tunes BuschiniI; Elaine PittnerII; Tiago CzervinskiII; Ivonete de Fátima MoraesI; Mônica Monteiro MoreiraIII; Hermes Francisco SanchesII; Marta Chagas MonteiroII
IDepartamento de Biologia do UNICENTRO
IIDepartamento de Farmácia do UNICENTRO
IIIDepartamento de Ensino do CEFET
The most common infections in human beings are caused by intestinal parasites. They can lead to a number of harmful effects, which could include, among others, intestinal obstruction, malnutrition, iron deficiency anemia, diarrhea, and poor absorption. In Brazil, enteroparasites are one of the main public health issues. The present study aims at analyzing the distribution and frequency of enteroparasite occurrence in 635 children from seven community schools in the city of Guarapuava, Paraná (PR). In addition, we used similarity and diversity indices to analyze the parasite community. We found 475 samples with at least one parasite showing that 75.27% of children had enteroparasites. A smaller fraction (26.73%) of children harbored several parasites (multiparasitism), especially Giardia duodenalis (56%), and Ascaris lumbricoides (18%). Statistical analysis showed that three (out of seven) children communities had higher similarity in frequency and amount of parasites. Our results suggest that the children studied were highly infected by enteroparasites. These levels of infestation could be related to several factors, such as climate, social and economic conditions and characteristics of the parasites.
Keywords: Enteroparasites. Ascaris lumbricoides. Giardia duodenalis. Multiparasitism. Ecology of parasites.
As infecções mais freqüentemente encontradas em seres humanos são ocasionadas por parasitos intestinais, os quais podem causar danos aos hospedeiros, que incluem, entre outros agravos, a obstrução intestinal, desnutrição, anemia por deficiência de ferro, quadros de diarréia e de má absorção. No Brasil, as enteroparasitoses estão entre os principais problemas de saúde pública. Este trabalho teve como objetivo avaliar a distribuição e freqüência de enteroparasitos em 635 crianças pertencentes a sete comunidades escolares do município de Guarapuava PR. Além disso, verificar índices de similaridade e diversidade de parasitas nas comunidades. Nos resultados, foram encontradas 475 amostras positivas para pelo menos um parasito, cuja prevalência de enteroparasitoses nesta população foi de 75,27 % e a ocorrência de casos de poliparasitismo de 26,73 %, dos quais foram registrados maiores índices de infecções por Giardia duodenalis (56 %) e Ascaris lumbricoides (18 %). A análise estatística mostrou que três das sete comunidades avaliadas apresentaram maior índice de similaridade quanto à freqüência e carga parasitária. Nossos resultados sugerem que as crianças avaliadas apresentavam altos índices de infecção por enteroparasitas e que fatores como clima, condições sociais e econômicas da população estudada e características próprias do parasito podem estar facilitando o acometimento destes indivíduos.
Palavras-chaves: Enteroparasitas. Ascaris lumbricoides. Giardia duodenalis. Poliparasitismo. Ecologia parasitária.
Parasitologic infections are among the leading disorders that affect school children in poor neighborhoods of urban centers1. In Brazil, enteroparasite infestations are one of the main public health problems2,3, especially when we take into account the great number of affected individuals and the several organic alterations caused by these infestations, including effects on nutritional status, growth and the cognitive function of students1.
The World Health Organization (WHO) estimates that diseases associated with poverty account for 45% of the total disease burden in developing countries3. Several studies have been conducted in the south Brazil in order to identify etiological agents associated with the epidemiological features of the disease4-7. In previous studies, we reported that 32.14% of children hospitalizations, in the city of Guarapuava, had been caused by intestinal parasitic infestation, mainly Ascaris lumbricoides7.
The most common intestinal helminthes found in human intestines are: Ascaris lumbricoides, Trichuris trichiura and ancylostomids: Necator americanus and Ancylostoma duodenale, whereas Entamoeba histolytica and Giardia duodenalis are the most common among protozoans. It has been estimated that one billion individuals around the world are infected by Ascaris lumbricoides, followed by Trichuris trichiura and ancylostomids8. Additionally, there are approximately 200 and 400 million people hosting Giardia duodenalis and Entamoeba histolytica, respectively9.
Previous studies investigated how the distribution of parasites in hosts could affect their causes and consequences10. In this context, it is crucial to investigate the diversity of parasites in different communities in order to understand their distribution patterns, which can be related to various factors, such as age, genetic characteristics, feeding habits, hosts' living conditions and interactions among parasite species11, 12. The constancy of parasite communities in the ecosystem will depend on the relationship between the growth rate of the host population and parasite pathogenicity. In order to survive in the environment, the growth rate should be significantly higher than pathogenicity11.
The main pathologic consequences caused by the disruption in the host-parasite relationship are: poor absorption, chronic diarrhea, anemia, malnutrition, abdominal pain, learning difficulties, poor concentration, and growth delay, which will result in lower efficiency in school13. High loads of parasites in the intestines can cause a reduction in nutrient penetration and intestinal absorption, an increase in catabolism, consumption of nutrients required for tissue growth and synthesis, induction of intestinal bleeding, intestinal obstruction, and rectum descent, and abscess formation14. Usually, clinical manifestations are directly related to the parasite load hosted by the individual15.
In this context, our study aimed at assessing ecological and epidemiological aspects of enteroparasites found in groups of students of several schools, such as: frequency of occurrence and enteroparasite distribution, similarity and diversity of enteroparasites in schools and the relationship between multiparasitism and age.
Material and methods
The survey of cases of parasitism in schools was conducted from March to November, 2004, in the city of Guarapuava, state of Paraná (PR). The current work reports the results obtained in an extension project conducted by the department of Pharmacy of the 'Universidade Estadual do Centro-Oeste (UNICENTRO)', with the support of the Culture, Education and Health authority of the city of Guarapuava.
The municipality of Guarapuava is located in the center-south region of the state of Paraná, an area of 3,125,852 km2. The estimated number of inhabitants is 155,161, with 141,694 living in urban and 13,467 in rural areas. The poverty index is 24.85%, with 44,787 people living in unfavorable conditions. Moreover, socioeconomic indicators show that Guarapuava has a Human Development Index (HDI) of 0.773, occupying the 82nd position in poverty of the total 399 cities of the state of Paraná16.
We selected seven communities (map below), where we collected the following number of feces samples: 95 samples at São Luiz (SL), 37 at Primavera (P), 49 at Karen (K), 79 at Xarquinho (X), 123 at Guaratu (G), 67 at Ampliando Horizonte (AH), and 25 at Vila Carli (VC). We chose these communities because they are the first areas where agents of the Family Health Program (Programa Saúde da Família, PSF) started their visits. The communities studied are the poorest and least urbanized areas in the city of Guarapuava. The poverty of these communities is favored by poor sanitary conditions, climate, lack of information, lack of access to healthcare, inadequate nutrition, and poor personal hygiene6, 7.
Once family members agreed to participate in the research, we interviewed them to determine gender, age and frequency in which raw greens were ingested and the water source they were using. After that, we gave each student a plastic vial to store a stool sample. Finally, along the development of the project we offered educational seminars on sanitation to parents and teachers, and taught them how to proceed when colleting fecal samples.
A total of 631 children (353 boys and 278 girls) from day nurseries and schools, ranging from zero to fifteen years of age, took part in the study. The parasitological tests were performed at UNICENTRO's Parasitology Laboratory. Due to the great number of daily samples, we used Hoffman, Pons and Janer free sedimentation methods17, 18, with three microscope slide readings for each sample.
Outcomes of these tests were later reported to the city Health Department. Children with positive results were treated and their families received orientation on PSF agents. This project was approved by the Research Ethics Committee of Universidade Estadual do Centro-Oeste and the participants in this study had no conflict of interest.
We used the Jaccard index19 to identify similarity patterns among school communities regarding the presence or absence of enteroparasites. A cluster analysis using the Bray Curts index19 was applied to distinguish differences among samples in terms of parasite abundance. The Shannon-Wiener (H') index, followed by a post-hoc t-test, was used to determine differences in the parasite diversity among school communities. Finally, we used the Chi-square test to evaluate differences in the abundance of each parasite species (in terms of percentage) among the communities studied (95% of significance).
A total of 475 (75.27%) samples of feces (out of 631 children belonging to seven school communities) had positive results, i.e., they harbored enteroparasites. The analysis of the parasite distribution among studied communities showed that all of them had more than 50% of their samples with parasites (Table 1).
Table 2 shows the distribution and frequency of enteroparasite occurrence among the seven school communities. We can see that Giardia duodenalis (356, 74.94%) and Ascaris lumbricoides (119, 25.05%) were significantly more frequent (Chi-square, p< 0.05) in the communities studied when compared to other parasites. Moreover, the majority of children (95%) ingested raw greens and drank tap water, whereas only a small fraction (5%) drunk well water (data not reported).
We built a dendogram based on Jaccard values that shows the similarity among school communities according to the presence and absence of parasites (Figure 1). On this representation, greater values correspond to higher similarity among school communities. The Jaccard index showed that the school communities SL and G had the highest similarity regarding parasite occurrence among their students (JI = 0.846), followed by SL and AH schools (JI = 0.769), and G and AH schools (JI = 0.769). In contrast, P and K schools had the lowest Jaccard value (JI = 0.333), i.e. both communities had little similar results between each other when compared to the other communities.
In another dendogram, based on parasite abundance per student (Figure 2), we could identify two groups: one pools together schools with higher parasite abundance (SL, X, G) and the other includes schools with lower student parasite abundance. (P, AH, K, VC). Shannon-Wiener (H') index showed that communities VC (H': 1.5263) and AH (H: 1.5176) had the highest enteroparasite diversity, whereas community K (H: 1.0476) had the lowest one.
The comparison between mono and multiparasitism in the seven school communities demonstrated that multiparasitism is common among the children studied. A total of 127 (26.74%) of them, out of 475 with positive results, were infected with more than one intestinal parasite. The community named 'Primavera' had the highest proportion of children with multiparasitism (32.43%), whereas the remaining communities had levels of multiparasitism ranging from 20% to 30% (Table 3).
Enteroparasite infestation rates are an important indicator of the sanitary conditions in which a certain population lives. The population under five years of age is a good indicator of local contamination because they have lower mobility and higher vulnerability20, 21. In the current study, we detected a high rate (75.27%) of enteroparasite occurrence in children attending seven school communities in the city of Guarapuava, State of Paraná (Table 1). According to the dendogram (Figure 1), the communities with the highest parasite abundance were SL, X and G. We believe this alarming scenario strongly reflects the effects of poor basic sanitary conditions (including tap water and sewage system) found in the municipality, which causes this high level of contamination and intestinal infestations. It is worth noting that basic sanitation is one of the main factors that cause some of the most important human diseases, including ascariasis and diarrhea22, 23. Recently, we reported some risk factors and nutritional status of children with intestinal parasites in a public nursery in the city of Guarapuava. These studies demonstrated that only 36% of the children washed their hands, approximately 50% walked without shoes; moreover, 50% of the children had eliminated worms in the past and 45% presented abdominal cramps6.
The parasites most frequently found in school children were Giardia duodenalis (56.41%) and Ascaris lumbricoides (18.85%) (Table 2). Similar results were reported in parasitological studies elsewhere, which pointed out that giardiasis is one of the main intestinal parasites among Brazilian children21,24,25. In Brazil, the infestation rate by Giardia changes according to the population and the region investigated. Giardiasis affects approximately 10 to 15% of the world population, whereas in Brazil this disease occurs in 9 to 50% of the population, affecting especially children above five years of age9,22. Giardiasis outbreaks are not rare, especially in day care centers and institutional populations25,26. Transmission of G. duodenalis can occur via water and food contaminated with cysts, and direct personal contact. Cysts are highly resistant, remaining viable for up to two months. Water treatment using chloride and heating to 60ºC has proven to be ineffective for inactivating cysts26. The prevalence of G. duodenalis infestation was strongly associated with a variety of risk factors including host, sociodemographic, environmental, and zoonotic27. This data can explain the high prevalence of Giardia in these children, mainly because the communities studied are in the poorest and least urbanized areas in the city of Guarapuava. The poverty of these communities is favored by poor sanitary conditions, climate, lack of information, lack of access to healthcare, inadequate nutrition, and poor personal hygiene6,7. In addition, we found that most children in this study (95%) drank tap water and ate raw greens, facts that favor parasite dissemination.
Several studies conducted in kindergarten and primary schools showed a high prevalence of intestinal infection by Ascaris lumbricoides2,7. In the municipality of Duque de Caxias (state of Rio de Janeiro), A. lumbricoides prevalence was estimated be 27.5% of the population. This data were obtained from a cropologycal and parasitological survey of 1,664 children with ages ranging from 1 to 9 years28. The spread of helminthiasis in Brazil is closely associated to humidity. A. lumbricoides infestations can be enhanced by high humidity, because their eggs are not able to infect the definitive host when they are released directly to the soil by their host's feces22. Infection only occurs after the developmental process that lasts approximately three to four weeks. During this period, they need hot, humid and shady substrates, where food and water will be contaminated22 This fact could explain the high prevalence of A. lumbricoides found in this study, since the city of Guarapuava has a mesotermic climate, wet and hyper-wet, with mild summers and no dry season29. Moreover, the high prevalence of A. lumbricoides is associated with poor sanitation conditions, which plays a crucial role in the health status of the population. Many factors can regulate this prevalence: geographical area, type of community (open or closed), social and economic status, access to goods and basic needs, nutrition, age and predisposition to infection by parasites30. Recently, we reported that 32.14% of children admissions in the city of Guarapuava, during the period from August 2002 to September 2006, were caused by Ascaris lumbricoides infestations. Moreover, the majority of children were between 0 to 3 years of age, had a nutritional deficit, and A. lumbricoides elimination7.
Studies conducted in Brazil pointed out that food contamination by helminthes and protozoans could be due to the ingestion of raw greens grown in areas with fecal contamination. Greens can be infected by transmissible forms of enteroparasites in several circumstances, from plantation to consumption. Besides, drinking water can be contaminated even after treatment8,31,32. Diseases caused by parasites still play a major role in the morbidity and mortality rates of several Brazilian regions, even in areas traditionally considered as the most developed in the country, such as the southeastern and southern regions. In this context, we noted that the majority of individuals studied used tap water and ate raw greens (data not reported). These factors could be important vectors to disseminate cysts, eggs and larvae. This problem could be solved with the use of portable water filtration units, the installation of cesspools and sewer systems to avoid the use of infected water for irrigation and washing, and more careful handling of greens from harvest for the preparation in school kitchens, houses or other locations31.
In order to evaluate the similarity among species in the communities, we observed that the SL, G and AH communities presented higher similarity among parasite species. In the past few years, researchers working with public health have been investigating the causes and consequences of parasite distribution in their hosts or communities. In this context, they noticed that variations in the aggregation of parasite patterns are correlated to the aging of hosts10. However, other factors can also lead to variations in parasite aggregation as a function of host age, such as i) temporal variation in the average infection rate, ii) parasite life expectancy and host predisposition to infection33, iii) host aggregation when exposed to parasite, which depends on behavior and host age 34 and iv) sampling errors35. Probably, these two last factors can explain better the high prevalence of enteroparasites among school children. We did not observe in our data any correlation between age and parasite aggregation (data not reported). Few studies have reported the association between number of parasites and host age, probably because this issue is usually not taken into account in these investigations12.
Another aspect to be highlighted is the high occurrence of multiparasitism in the individuals investigated in this study (Table 5). In the city of Barra de Santo Antônio, state of Alagoas, out of a total of 1,020 students examined, 983 (92%) showed positive results for at least one species of parasite; 171 (18.2%) individuals were infected by just one parasite; and 767 (81.8%) presented multiparasitism, harboring up to eight different species. The helminthes most frequently found were Trichuris trichiura, Ascaris lumbricoides and Ancilostomatidae36. Similar results were found elsewhere. In the city of Tacaratu, state of Pernambuco, extremely high rates of parasite infestations were found, as well as the occurrence of multiparasitism. The most common species was Entamoeba histolytica, which infected on average 82.4% of family members in every household. This parasite infection occurred in almost all adults (95.3%) and 40.7% of the children from 0 to 4 years old. The Ascaris lumbricoides parasite was the second most frequent, affecting on average 51.2% of the population, especially children under 15 years of age. In this age range, (62.0%) the number of individuals infected by Giardia duodenalis, was also high, with at least three different species for each family37. At the city of Gerbi Estiva (state of São Paulo), the highest incidence of parasites among students was due to the commensal protozoan Entamoeba coli, which occurred in 5.2% of the children infected (n=47), followed by Giardia duodenalis (5.0%, n=45), Ascaris lumbricoides (1.5%, n=14), and Endolimax nana (0.8%, n=08). Other parasites had lower incidence rates, but there was a wide array of intestinal parasites affecting the population studied, including Enterobius vermicularis (0.2%), Hymenolepis nana, (0.1%), Trichuris trichiura (0.1%), and ancylostomids: Ancylostoma duodenalis and Necator americanus. Ancylostomatidaes could not be distinguished in the fecal exams but they had clinical and epidemiological incidence (0.1%). These results were pooled separately among the several schools according to the number of positive cases38. Based on the current data, we can suggest that programs to control parasitism should give priority to children attending school, which represent a vulnerable group showing faster growth in endemic countries. The alarming scenario showed in the present study highlights the need to identify, treat and prevent parasitological infestations in order to avoid likely outbreaks and the formation of new endemic areas. It is worth observing that preventive measures to control parasitological diseases will contribute to reduce annual expenditure on specific treatments13.
We concluded that children attending school in the city of Guarapuava are highly infected by enteroparasites. Also, the incidence of the parasites Ascaris lumbricoides and Giardia duodenalis could be related to several factors that help their dissemination, such as climate, social and economic conditions of the studied population and specific parasite features, which facilitate school children infestations. Moreover, we claimed that lack of hygiene and basic sanitation could play a major role in parasite dissemination, causing several health problems in these children.
1. Prado MS, Barreto ML, Strina A, Faria JAS, Nobre AA, Jesus SR. Prevalência e intensidade da infecção por parasitas intestinais em crianças na idade escolar na Cidade de Salvador (Bahia, Brasil). Rev Soc Bras Med Trop 2001; 34 (1): 99-101.
2. Almeida JÁ, Araújo MBM, Rodrigues MLPR, Reis MA, Teixeira, VPA. Prevalência de enteroparasitoses em fezes colhidas durante necropsias. Rev Soc Bras Med Trop 1991; 24: 27-9.
3. World Health Organization: World Health Report 2002. Geneva; 2002.
4. Scolari C, Torti C, Beltrame A, Matteelli A, Castelli F, Gulletta M, Ribas M, Morana S, Urbani C. Prevalence and distribution of soil-transmitted helminth (STH) infections in urban and indigenous schoolchildren in Ortigueira, State of Paraná, Brasil: implications for control. Trop Med Int Health 2000; 5(4): 302_7.
5. Ogliari T CC, Passos JT. Enteroparasites in students of fifth series of "Colegio Estadual de Terra Boa" Campina Grande do Sul, Paraná (southern Brazil). Acta Biol Par 2002; 31: 65-70.
6. Ferreira H, Lala ERP, Monteiro MC, Raimondo ML. Estudo epidemiológico localizado da freqüência e fatores de risco para enteroparasitoses e sua correlação com o estado nutricional de crianças em idade pré-escolar: parasitoses intestinais e desenvolvimento infantil. Publ UEPG Ciênc Biol Saúde 2006a; 12(4): 33-40.
7. Ferreira H, Lala ERP, Czaikoski PG, Buschini MLT, Monteiro MC. Enteroparasitoses e déficit nutricional em crianças hospitalizadas, Guarapuava, Estado do Paraná, Brasil. Acta Sci Health Sci 2006b; 28(2):113-7.
8. Crompton DWT. The prevalence of Ascariasis. Parasitol Today 1988; 4: 162-9.
9. Vidal AMB, Catapani WR. Enzyme-linked immunosorbent assay (ELISA) immunoassaying versus microscopy: advantages and drawbacks for diagnosing giardiasis, Sao Paulo. Med J 2005; 123(6): 282-5.
10. Anderson, R.M., Gordon, D.M. Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 1982; 85: 373-98.
11. Dobson, A.P. Models for multi-species parasite-host communities. In: The Structure of Parasite Communities (eds Esch, G., Kennedy, C.R., Aho, J.) London: Chapman and Hall; 1990. p. 261-88.
12. Von Zuben, C. Implicações da agregação espacial de parasitas para a dinâmica populacional na interação hospedeiro-parasita. Rev Saúde Pública, 1997; 31: 523-30.
13. Vinha C. Necessidade de uma política sanitária nacional para o combate as parasitoses intestinais. Rev Soc Bras Med Trop 1976; 10: 297-301.
14. Castiñeiras TMPP e Martins, FSV. Infecções por helmintos e enteroprotozoários. Centro de Informação em Saúde para Viajantes Cives (www.cives.ufrj,br); 2003.
15. Stephenson LS. The impact of helminth infestations on human nutrition. London: Taylor & Francis;1987.
16. Instituto Paranaense de Desenvolvimento Econômico e Social. Disponível em: http://www.ipardes.gov.br/index. (Acessado em 13 de setembro de 2007)
17. Hoffmann, W.A.; Pons, J.A.; Janer, J.L. The sedimentation concentration method in schistosomiasis mansoni. P R J Public Health Trop Med 1934; 9: 281-98.
18. Lutz, A. O Schistosoma mansoni e a schistosomatose segundo observações feitas no Brasil. Memórias do Instituto Oswaldo Cruz 1919; 11: 121-55.
19. Luidwig, J.A. and Reynolds, J.F. Statistical Ecology. New York: John Wiley & sons; 1988.
20. UNICEF (Fundo das Nações Unidas para a Infância), Situação Mundial da Infância. Brasília: Unicef; 1995.
21. Cardoso GS, Santana ADC, Aguiar CP. Prevalência e aspectos epidemiológicos da giardíase em creches no município de Aracaju, SE, Brasil. Rev Soc Bras Med Trop 1995; 28: 25-31.
22. Gross R, Schell B, Molina MCB, Leão MAC, Strack U. The impact of improvement of water supply and sanitation facilities on diarrhea and intestinal parasites: a Brazilian experience with children in two low-income urban communities. Rev Saúde Pub 1989; 23: 214-20.
23. Esrey SA, Potash JB, Roberts L. Effects of improved water supply and sanitation on ascaris diarrheas, dracunculiasis, hookworm infection, schistosomiasis and trachoma. Bulletin of the World Health Organization 1991; 69: 609-21.
24. Berbert-Ferreira M, Costa-Cruz JM, Moraes MMAR, Cardoso MLG, Oliveira AM. Parasitas intestinais em pré-escolares da escola de Educação Básica da Universidade Federal de Uberlândia, Minas Gerais no ano de 1989. Rev C Ciênc Biom Univers Fed Uberlândia 1990; 6: 15-9.
25. Teixeira JC; Heller L; Barreto ML. Giardia duodenalis infection: risk factors for children living in sub-standard settlements in Brazil. Cad Saúde Pública 2007; 23(6): 1489-93.
26. Ortega, J.R.; Adam, R.D. Giardia: overview and update. Clin Infectious Diseases 1997; 25: 545-50.
27. Pereira MGC, Atwill ER, Barbosa AP. Prevalence and associated risk factors for giardia lamblia infection among children hospitalized for diarrhea in Goiânia, Goiás state, Brazil. Rev Inst Med Trop S. Paulo 2007; 49(3): 139-45.
28. Campos MR, Valencia LIO, Fortes BPMD, Braga RCC, Medronho RA. Distribuição espacial da infecção por Ascaris lumbricoides. Rev Saúde Pública 2002; 36(1): 69-74.
29. Thomaz EL, Vestena LR. Aspectos Climáticos de Guarapuava PR. Guarapuava: Editora UNICENTRO; 2003.
30. Holveck JC, Ehrenberg JP, Ault SK, Rojas R, Vasquez J, Cerqueira MT, Ippolito-Shepherd J, Genovese MA, Periago MR. Prevention, control, and elimination of neglected diseases in the Americas: Pathways to integrated, inter-programmatic, inter-sectoral action for health and development. BMC Public Health 2007, 7: 1-21.
31. Coelho LMPS, Oliveira SM, Milman MHSA, Santos RP. Detecção de formas transmissíveis na água e nas hortaliças consumidas em comunidades escolares de Sorocaba, São Paulo, Brasil. Rev Soc Bra Med Trop 2001; 34(5): 479-82.
32. Guimarães AM, Alves EGL, Figueiredo HCP, Costa GM, Rodrigues LS. Freqüência de enteroparasitas em amostras de alface (Lactuca sativa) comercializadas em Lavras, Minas Gerais. Rev Soc Bras Med Trop 2003; 36(5): 621-3.
33. Quinnel, R. et al. Changes in parasite aggregation with age: a discrete infection model. Parasitology 1995; 111: 635-44.
34. Woolhouse, M.E.J. et al. On the interpretation of intensity of infection data for Shistosoma haematobium. Trans R Soc Trop Med Hyg 1994; 88: 520-6.
35. Pacala, S.W.; Dobson, A.P.. The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology 1988; 96: 197-210.
36. Fontes G, Oliveira KKL, Oliveira AKL, Rocha EMM. Influência do tratamento especifico na prevalência de enteroparasitoses e esquistossomose em escolares do município de Barra de Santo Antônio, AL. Rev Soc Bras Med Trop 2003; 36(5): 625-8.
37. Fontbonne A, Freese-De-Carvalho E, Acioli MD, Sá GA, Cesse EAP. Fatores de risco para poliparasitismo intestinal em uma comunidade indígena de Pernambuco, Brasil. Cad Saúde Pub 2001; 17(2): 367-73.
38. Ferreira GR., Andrade CFS. Alguns aspectos socioeconômicos relacionados a parasitoses intestinais e avaliação de uma intervenção educativa em escolares de Estiva Gerbi, SP. Rev Soc Bras Med Trop 2005; 38(5): 402-5.
Profa. Dra. Marta Chagas Monteiro
Address: Depto. de Farmácia/CCS
Rua Simeão Camargo Varela de Sá, 03. Cascavel
Phone: 42-3629-8137. Fax: 42-3629-8100.
Recebido em: 04/04/07
Versão final reapresentada em: 18/09/07
Aprovado em: 24/09/07